Published online before print January 25, 2007, doi: 10.1161/01.ATV.0000258795.75121.8a
© 2007 American Heart Association, Inc.
Vascular Biology |
Carbamylated Low-Density Lipoprotein Induces Monocyte Adhesion to Endothelial Cells Through Intercellular Adhesion Molecule-1 and Vascular Cell Adhesion Molecule-1
From the Division of Nephrology (E.O.A., S.V.S., E.O., A.G.B.), Department of Internal Medicine, University of Arkansas for Medical Sciences, Little Rock, Ark; Renal Medicine Service (S.V.S., A.G.B.), Central Arkansas Veterans Healthcare System, Little Rock, Ark; Division of Nephrology (E.O.), Department of Internal Medicine, Ege University Medical School, Izmir, Turkey.
Correspondence to Alexei G. Basnakian, Division of Nephrology, Department of Internal Medicine, University of Arkansas for Medical Sciences, 4301 W. Markham St, Slot 501, Little Rock, AR 72205. E-mail basnakianalexeig{at}uams.edu
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Abstract |
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Objective— Carbamylated low-density lipoprotein (LDL), the most abundant modified LDL isoform in human blood, has been recently implicated in causing the atherosclerosis-prone injuries to endothelial cells in vitro and atherosclerosis in humans. This study was aimed at testing the hypothesis that carbamylated LDL acts via inducing monocyte adhesion to endothelial cells and determining the adhesion molecules responsible for the recruitment of monocytes.
Methods and Results— Exposure of human coronary artery endothelial cells with carbamylated LDL but not native LDL caused U937 monocyte adhesion and the induction of intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 adhesion molecules as measured by cell enzyme-linked immunosorbent assay. Silencing of intercellular adhesion molecule-1 by siRNA or its inhibition using neutralizing antibody resulted in decreased monocyte adhesion to the endothelial cells. Similar silencing or neutralizing of vascular cell adhesion molecule-1 alone did not have an effect but was shown to contribute to intercellular adhesion molecule-1 when tested simultaneously.
Conclusions— Taken together, these data provide evidence that intercellular adhesion molecule-1 in cooperation with vascular cell adhesion molecule-1 are essential for monocyte adhesion by carbamylated low-density lipoprotein-activated human vascular endothelial cells in vitro.
The exposure of human coronary artery endothelial cells with carbamylated LDL but not native LDL caused U937 monocyte adhesion and the induction of ICAM-1 and VCAM-1 adhesion molecules. Silencing of ICAM-1 and VCAM-1 by siRNA or their inhibition using neutralizing antibody resulted in decreased monocyte adhesion to the endothelial cells.
Key Words: atherosclerosis • carbamylated low-density lipoprotein • endothelial cells • intercellular adhesion molecule-1 • monocyte adhesion • vascular cell adhesion molecule-1
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Introduction |
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Monocyte (leukocyte) adhesion to activated vascular endothelial cells and their migration into the vessel wall is the critical event in the initiation of atherosclerosis. This process is caused by the upregulation of adhesion molecules on endothelial cells and an increased expression in the vascular wall of chemotactic factors to monocytes. Highly specific adhesive interactions between monocytes and endothelial cells are mediated by 3 main families of receptors: members of the immunoglobulin superfamily, selectins, and integrins. Recent studies indicate that intercellular adhesion molecule-1 (ICAM-1) and vascular cell adhesion molecule-1 (VCAM-1), members of the immunoglobulin superfamily, are the most common participants in monocyte attraction induced by different stimuli.1–3 The expression of adhesion molecules and monocyte adhesion can be triggered by a variety of plasma components, such as interferon-
,4 homocysteine,5 and lipoproteins, like oxidized low-density lipoprotein (oxLDL),6 or its derivates, oxidized 1-palmitoyl-2-arachidonoyl-sn-glycero-3-phosphocholine7 and lysophosphatidylcholine.8 The identification of new plasma components that are responsible for monocyte adhesion is important in light of their potential application as pathogenic atherosclerosis markers, predictors or therapeutic targets. Carbamylated low-density lipoprotein (cLDL) is a recently identified type of modified low-density lipoprotein (LDL) that seems to be important in atherosclerosis in humans.9–11 It is generated by irreversible chemical modification of the protein component of the LDL particle, apolipoprotein B, and by urea-derived cyanate present in human blood plasma.9 Plasma levels of cLDL as determined by sandwich enzyme-linked immunosorbent assay (ELISA) methods vary in a higher range of concentrations than oxLDL, which makes it the most abundant LDL isoform of human plasma.11 The elevation of blood urea in uremic patients causes a proportional increase of plasma cLDL.11 The LDL of chronic renal failure patients on dialysis was shown to induce greater monocyte–endothelial cell adhesion.12 A higher level of plasma cLDL correlates with atherosclerosis in uremic patients.13 Our recent study showed that cLDL induced a variety of damaging stimuli to endothelial and vascular smooth muscle cells, all of which are attributed to atherosclerosis.10,14 These include incorporation by endothelial cells, cytotoxicity toward endothelial cells, and the induction of vascular smooth muscle cell proliferation.
The present study was undertaken to determine whether monocyte adhesion to endothelial cells can be induced by cLDL and to identify the adhesion molecules involved in this process. This in vitro study utilizes U937 monocyte cells and human coronary artery endothelial cells (HCAECs), commonly used for studies of monocyte adhesion.3,10 We demonstrated that cLDL induces ICAM-1 and VCAM-1 on endothelial cells, and the role of these adhesion molecules in the attraction of monocytes in vitro. Inactivation of these pathways by RNA interference or inhibiting the antibody strongly protected against the adhesion of monocytes to endothelial cells, thus providing evidence for the potential importance of these mechanisms in cLDL-mediated atherosclerosis.
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Materials and Methods |
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An expanded materials and methods section is available online (please see http://atvb.ahajournals.org).
Native, cLDL, and oxLDLs
Native human LDL (nLDL) and all chemicals were purchased from Sigma (St. Louis, Mo) unless designated otherwise. The cLDL was prepared as previously described by us.10,11 The oxLDL was prepared as described by Kume et al15 and used as a positive control.
Monocyte Adhesion
The U937 cells were chosen because they have the phenotype of the monocytes and are commonly used in monocyte adhesion studies.3,5,6 Monocyte adhesion was determined as described by Koga et al.16
Monocyte adhesion to cLDL-activated HCAECs under flow conditions was performed similarly to methods described elsewhere.17
Cell ELISA
Cell ELISA was performed as described by Frahm et al.18 Antibody titers and optimal reaction conditions were elaborated before the experiment.
Immunocytochemistry
Immunocytochemical staining of LDL-treated cells with polyclonal anti–ICAM-1 (1:100) or anti–VCAM-1 (1:100) antibody (Santa Cruz Biotechnology) was performed similarly as that described by Langer et al.19
ICAM-1 and VCAM-1 siRNA Silencing
For the study of protection from monocyte adhesion, HCAECs were transfected with siRNA to ICAM-1, VCAM-1, or both for 48 hours, then the transfection medium was removed, and the cells were treated with cLDL or vehicle in serum-free medium for 24 hours.
RNA Extraction and Real-Time Reverse-Transcription Polymerase Chain Reaction
The total RNA was extracted using a RNeasy Mini kit from Qiagen (Valencia, Calif) as suggested by the manufacturer. The reverse-transcription reaction was performed using the GeneAmp Gold RNA PCR core kit (Applied Biosystems, Foster City, Calif) using Oligo d(T)16. The reaction mix was prepared using Platinum SYBR Green qPCR Supermix-UDG (Invitrogen Corporation, Carlsbad, Calif) according to manufacturer recommendations.
Statistical Analysis
The results were expressed as mean±SEM. The statistical analysis was performed using SPSS software (SPSS Inc, Chicago, Ill). To evaluate the significance of differences between the 2 groups of experiments, the ANOVA and Student t test were used. Additionally, to evaluate the significance of several time points in comparison to one control point, the Bonferroni adjustment of the t test was used. A value of P<0.05 was considered statistically significant.
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Results |
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Acceleration of Monocyte Adhesion to Endothelial Cells by cLDL
To determine whether cLDL causes monocyte adhesion to endothelial cells, cLDL (200 µg/mL) was applied to the endothelial cells for different periods of time and BCECF-AM–labeled U937 cells were allowed to adhere for 30 minutes. We found a significant increase of monocyte adhesion to the endothelial cells treated for 12 hours or longer with cLDL, whereas nLDL and the vehicle control did not cause any monocyte adhesion (Figure 1). The oxLDL that was previously described to induce monocyte adhesion,6,20,21 was used as a positive control. A 6-hour or longer treatment with oxLDL (200 µg/mL) caused a 4-fold increase of monocyte adhesion to the endothelial cells. It is interesting that once monocyte adhesion to oxLDL-treated endothelial cells reached the maximum, no further increase of adhesion was observed. Contrary to oxLDL, cLDL caused significant monocyte adhesion versus nLDL and vehicle control only after a 12-hour course, followed then by a further increase of monocyte adhesion over the level of oxLDL. At the end of the 24-hour course, the adhesion induced by cLDL was higher than the one induced by oxLDL.
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Our next step experiment showed that freshly isolated human monocytes also have higher rate of adherence to endothelial cells pretreated with both cLDL and oxLDL (Figure 2A, 2B). Further, to see whether modified LDL-activated endothelial cells still attract monocytes under flow conditions, the adhesion experiments using laminar flow chambers were performed (Figure 2C, 2D). Our results demonstrate that similar to static adhesion experiments with both U937 cells and freshly isolated monocytes, HCAECs treated with modified LDLs attract more monocytes than vehicle-treated or nLDL-treated cells.
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cLDL Induces ICAM-1 and VCAM-1 Expression in Endothelial Cells
We studied the expression of adhesion molecules, ICAM-1, VCAM-1, and P-selectin, and a chemokine, MCP-1, which could potentially mediate cLDL-induced monocyte adhesion to endothelial cells. HCAECs were treated with varying concentrations of cLDL or nLDL for 24 hours, and the expressions of adhesion molecules were determined using cell ELISA (Figure 3). The data showed that the expression of MCP-1 and P-selectin was not induced by the treatment with cLDL in comparison to nLDL. However, the expression of ICAM-1 and VCAM-1 was significantly increased by cLDL. ICAM-1 was induced to a higher degree then VCAM-1. Contrary to cLDL, oxLDL did not affect ICAM-1 and VCAM-1 expression, whereas expressions of P-selectin and, to a lesser extent, MCP-1 molecules were increased. The nLDL did not cause any significant change of either ICAM-1 or VCAM-1 expression.
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The results of cell ELISA regarding ICAM-1 and VCAM-1 expression after cLDL treatment was confirmed by immunocytochemistry: cLDL-treated HCAECs expressed significantly more ICAM-1 and VCAM-1 in comparison to the vehicle control or nLDL-treated cells (Figure 4).
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To determine whether the observed induction of ICAM-1 and VCAM-1 is present at the level of transcription, real-time PCR was performed with RNA extracted from the vehicle-treated, cLDL-treated (200 µg/mL), or nLDL-treated (200 µg/mL) endothelial cells. Our results suggest that the transcription of both studied molecules was upregulated at 4 and 8 hours (supplemental Figure I, available online at http://www.atvb.ahajournals.org). The mRNA expression of both molecules was decreasing at later time points.
ICAM-1 and VCAM-1 Mediate cLDL-Induced Monocyte Adhesion to Endothelial Cells
To determine whether cLDL-induced ICAM-1 and/or VCAM-1 overexpression cause the adhesion of monocytes to endothelial cells, 2 approaches were applied. In the first, we abolished the function of ICAM-1 and VCAM-1 with antibodies, and in the second, the expression of these adhesion molecules was silenced by using siRNA.
Because of the superficial location of adhesion molecules in the endothelium, the antibodies to these proteins are widely used to determine the role of adhesion molecules in endothelial cells.5,22 Our experiments showed that the inhibition of ICAM-1 caused a significant 
30% reduction of monocyte adhesion to endothelial cells, whereas the inhibition of VCAM-1 had only a minor and nonsignificant effect (Figure 5). In the same experiment, simultaneous pretreatment of endothelial cells with both anti–ICAM-1 and anti–VCAM-1 antibodies caused the most significant inhibition of monocyte adhesion (60%). Rabbit -immunoglobulins used as a negative control did not have a significant effect on monocyte adhesion regardless of the treatment.
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Before using RNA interference, we determined the optimal conditions for siRNA transfection using siRNA-fluorescein isothiocyanate and specific siRNA, because HCAECs are notoriously difficult cells to transfect.23 These experiments showed that the optimal conditions for siRNA transfection to the endothelial cells are 60% to 70% confluence with a transfection time of no more then 48 hours. These conditions allowed reaching a transfection level of up to 70% to 80% (supplemental Figure IIA). The introduction of the specific siRNA resulted in a significant inhibition of ICAM-1 or VCAM-1 expression in modified LDL-treated cells as determined using real-time reverse-transcription polymerase chain reaction (supplemental Figure IIB).
After the application of siRNAs to the HCAECs for 48 hours, the cells were treated for an additional 16 hours with vehicle, cLDL, or nLDL and monocyte adhesion was measured as described in the Methods section. The data presented in Figure 6 show that cLDL caused accelerated monocyte adhesion to endothelial cells, and it was significantly suppressed by anti-ICAM-1 siRNA. Anti–VCAM-1 siRNA had only a partial effect while simultaneously using both anti–ICAM-1 and anti–VCAM-1 siRNAs caused the most prominent and significant suppression of monocyte adhesion. It did not reach the level of cells treated with the vehicle or nLDL, but it was consistent with the transfection efficiency observed in this experiment. Although nLDL did not accelerate monocyte adhesion, it was slightly suppressed by specific siRNAs. The control siRNA did not protect the endothelial cells from monocyte adhesion. These experiments provide evidence that ICAM-1 in cooperation with VCAM-1 is involved in monocyte adhesion by cLDL-activated human endothelial cells in vitro.
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Discussion |
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This study for the first time to our knowledge determined that cLDL induces the adhesion of monocytes to human vascular endothelial cells in vitro and identified the adhesion molecules, which are important in this process. The cLDL was demonstrated to induce ICAM-1 and VCAM-1 and had no effect on MCP-1 or P-selectin. These 4 molecules and some others were described before to be involved in the monocyte adhesion to the endothelium.24 As opposed to cLDL, oxLDL, the most studied modified LDL, was shown to induce the expression of P-selectin25 and MCP-1.26 There is conflicting evidence regarding the involvement of ICAM-1 and VCAM-1 in oxLDL-induced monocyte–endothelial adhesion. While some studies showed that oxLDL may cause the induction of ICAM-1 and VCAM-1 expression and monocyte adhesion,21,27 others suggested that oxLDL does not induce VCAM-128 or either one.26,29 In support of this, Khan et al observed no change in ICAM-1 or VCAM-1 expression as measured by ELISA of cultured HAECs or human umbilical vein endothelial cells that were incubated with oxLDL or glycated LDL.30 Our data suggest that oxLDL action is not mediated by ICAM-1 or VCAM-1. Therefore, our subsequent experiments were aimed to study cause–effect relationship between cLDL-induced expression of ICAM-1 and VCAM-1 and monocyte adhesion. We have shown that unlike the other modified LDLs, cLDL induces ICAM-1 and VCAM-1 in a dose-dependent manner. The protein increase of ICAM-1 and VCAM-1 was strongly associated with the mRNA increase and monocyte adhesion. Therefore, there is a possibility that cLDL is a more potent inducer of monocyte adhesion than other modified LDLs.
Both ICAM-1 and VCAM-1 protein expressions were increased after cLDL treatment in 16 to 24 hours, whereas the mRNAs of both molecules reached a maximum at the 8-hour point. In endothelial cells treated with lipoproteins, ICAM-1 and VCAM-1 mRNAs were previously shown to be induced within 2 to 8 hours after the impact and then to be downregulated, whereas the proteins are usually induced later, at 8 to 48 hours after treatments.31,32 Our results suggested that after cLDL treatment, the VCAM-1 expression was increased to a lesser degree then the expression of ICAM-1. These data are in agreement with other studies suggesting higher reactivity of ICAM-1 after exposure to exogenous factors, including LDL.6,30,31 Monocyte recruiting is a multistep process that consists of capture, rolling, activation, adhesion, and transmigration. Although the roles of ICAM-1 and VCAM-1 are known to be mainly in adhesion and transmigration, their inactivation may in some cases also affect rolling.24 We can speculate that cLDL is involved in all of these processes.
Using cause–effect relationship approaches by using specific siRNA or neutralizing antibodies, we found that ICAM-1 and VCAM-1 are the adhesion molecules responsible for the endothelial cell attraction of monocytes induced by cLDL. Our studies also indicate that ICAM-1 is more important for cLDL-induced monocyte adhesion than VCAM-1. Both siRNA and the utilization of neutralizing antibodies determined that silencing/neutralizing of ICAM-1 alone provided inhibition of monocyte adhesion to endothelial cells. VCAM-1 contributes to this process because the silencing or neutralizing of both molecules caused the maximal effect. To the best of our knowledge, reports on the use of specific anti-ICAM-1 or anti-VCAM-1 siRNA to study monocyte adhesion to endothelial cells are not available. Our observation of the predominance of ICAM-1 is in agreement with at least one previous study. Using the pretreatment of endothelium with anti-ICAM-1 and anti-VCAM-1 antibodies in a human ex vivo experiment, Crook et al reported that ICAM-1 participates in monocyte adhesion while the role of VCAM-1 is rather secondary and dependent on the degree of its expression in the endothelium.33 It is likely that cooperation between the molecules promotes monocyte adhesion. For example, monocyte adhesion induced by a high glucose concentration was inhibited by simultaneous use of anti–ICAM-1, anti–VCAM-1, and anti–CD-18 antibodies.34 Taken together with the previous study of cLDL cytotoxicity to HCAECs in vitro,10 it can be concluded that cLDL produces a variety of atherosclerotic-prone signals to endothelial cells. Some of these signals may be different from the effects of other modified LDLs.
Several experiments in this study use high concentrations of cLDL, 50 to 400 mg/L, which may raise a question whether these conditions are physiologically relevant. While several LDL modifications have been identified, only 2 of them, oxLDL and cLDL, can be precisely measured in human plasma using sandwich ELISAs. Malondialdehyde-modified LDL, an isoform of oxLDL, was detected in healthy individuals at 1.9±0.2 µg/mL,35 3.1±1.6 µg/mL,36 and 17.1±50.2 µg/mL.37 The oxLDL concentration was 0.5±0.3 U/µg38 or 10.8±2.8 U/mL39 LDL protein (1 U was 1 µg of mildly oxLDL). The cLDL concentration determined in our recent study showed a much higher value of 86.0±29.7 µg/mL.11 It reached 300 µg/mL in uremic patients with chronic renal failure, who are known to be predisposed to atherosclerosis. Therefore, the cLDL concentrations used in this study are physiologically meaningful.
Future studies may be focused on determining whether cLDL-induced adhesion results in increased rolling, arrest, and transmigration of monocytes.40 If observations from this study are confirmed in vivo, future therapeutic approaches may be aimed at the inhibition of ICAM-1 and VCAM-1 as protective measures to attenuate the progression of atherosclerosis. In this regard, using siRNA that we have tested or inhibiting the signal transduction pathways leading to induction of the adhesion molecules, for example, NF-
B–activating signaling pathways,41 would be highly appropriate.
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Acknowledgments |
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The authors thank Ray Biondo, MD, MS, for editorial assistance, and Anna G. Stewart for technical assistance.
Sources of Funding
This research was supported by a grant from Satellite Healthcare (A.G.B., S.V.S.), VA Merit review grants (A.G.B., S.V.S.), fellowships from the Turkish Nephrology Association and the International Society of Nephrology (E.O.), and an Arkansas Tobacco Settlement Award (E.O.A.).
Disclosure
None.
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Footnotes |
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Original received September 14, 2006; final version accepted January 5, 2007.
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